Download Green leaf volatiles: biosynthesis, biological functions and their

Plant Biotechnology Journal (2015) 13, pp. 727–739
doi: 10.1111/pbi.12368
Review article
Green leaf volatiles: biosynthesis, biological functions and
their applications in biotechnology
Muhammad Naeem ul Hassan1,2, Zamri Zainal1,3 and Ismanizan Ismail1,3,*
1
Faculty of Science and Technology, School of Bioscience and Biotechnology, University Kebangsaan Malaysia, Bangi, Malaysia
2
Department of Chemistry, University of Sargodha, Sargodha, Pakistan
3
Institute of Systems Biology (INBIOSIS), University Kebangsaan Malaysia, Bangi, Malaysia
Received 21 September 2014;
revised 25 February 2015;
accepted 25 February 2015.
*Correspondence (Tel +60389214546;
fax +603 8921 3398;
emails [email protected];
[email protected])
Keywords: lipoxygenase, hydroperoxy
lyase, oxylipin, jasmonic acid, tritrophic
interactions.
Summary
Plants have evolved numerous constitutive and inducible defence mechanisms to cope with
biotic and abiotic stresses. These stresses induce the expression of various genes to activate
defence-related pathways that result in the release of defence chemicals. One of these defence
mechanisms is the oxylipin pathway, which produces jasmonates, divinylethers and green leaf
volatiles (GLVs) through the peroxidation of polyunsaturated fatty acids (PUFAs). GLVs have
recently emerged as key players in plant defence, plant–plant interactions and plant–insect
interactions. Some GLVs inhibit the growth and propagation of plant pathogens, including
bacteria, viruses and fungi. In certain cases, GLVs released from plants under herbivore attack
can serve as aerial messengers to neighbouring plants and to attract parasitic or parasitoid
enemies of the herbivores. The plants that perceive these volatile signals are primed and can
then adapt in preparation for the upcoming challenges. Due to their ‘green note’ odour, GLVs
impart aromas and flavours to many natural foods, such as vegetables and fruits, and therefore,
they can be exploited in industrial biotechnology. The aim of this study was to review the
progress and recent developments in research on the oxylipin pathway, with a specific focus on
the biosynthesis and biological functions of GLVs and their applications in industrial
biotechnology.
Introduction
As plants are sessile organisms, they are constrained to use
structural and chemical defences against attack, and do so
without the benefit of having an animal-like immune system.
Nonetheless, plants are able to mount alternative strategies for
effective defence, which are comprised of constitutive, as well as
inducible, mechanisms against a variety of biotic and abiotic
stresses. Constitutive mechanisms include protective layers on
the exterior surface of plants, such as the cell wall, wax, bark and
trichomes, whereas inducible mechanisms include apoptosis,
production of proteins and release of defence chemicals. Plant
chemical defences are products of secondary metabolism and are
not directly involved in plant growth and development; however,
these chemicals perform specialized roles under specific environmental and physiological conditions. Plant secondary metabolites
not only serve as key players in the plant defence system, but
also they have other useful biological functions. In addition, these
low molecular weight organic compounds have industrial applications and are widely used as antioxidants, colourants, fragrants
and flavourants (D’Haeze and Holsters, 2002; Frydman et al.,
2004; Lange and Ahkami, 2013; Verdonk et al., 2003). These
chemicals are deployed by plants to prevent the potential
damage caused by herbivores and various pathogens, such as
bacteria, viruses and fungi. The biosynthesis of secondary
metabolites occurs through several metabolic pathways and
varies among plant communities, depending on the species,
environment and stage of development. The oxylipin pathway is
one of the most important pathways in which many defencerelated genes are activated to induce chemical defence
responses, which results in the synthesis of useful secondary
metabolites (Figure 1).
Phyto-oxylipins are a diverse class of bioactive lipids that are
derived by the oxidation of polyunsaturated fatty acids (PUFAs),
mainly linoleic acid (LA, 18:2 D9, 12) and a-linolenic acid (ALA,
18:3 D9, 12, 15). This class is represented by jasmonates,
divinylethers and green leaf volatiles (GLVs). Jasmonates include
12-oxo-phytodienoic acid (OPDA), jasmonic acid (JA) and methyl
jasmonate (MeJA), while GLVs consist of C6 and C9 aldehydes,
alcohols and their esters (Baldwin et al., 2006; Liechti and Farmer,
2006; Liechti et al., 2006; Matsui, 2006; Wasternack, 2007).
Jasmonates have been found to regulate various physiological
processes of plant development, such as embryogenesis, seed
germination, fruit ripening and leaf senescence, but these
compounds are particularly important because of their role in
plant defence and host immunity (Balbi and Devoto, 2008;
Heinrich et al., 2013; Kessler et al., 2004; Liechti and Farmer,
2003; Wasternack, 2007). GLVs are released under various stress
conditions to aid in plant defence against herbivory and bacterial
and fungal pathogens (Shiojiri et al., 2006a). In addition, GLVs
are a major component of the blend of volatiles used for
interplant communication (Engelberth et al., 2004; Gershenzon,
2007). Here, we review the basic components of and the recent
developments in the oxylipin pathway with a specific focus on the
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727
728 Muhammad Naeem ul Hassan et al.
Figure 1 Oxylipin pathway: Biosynthesis of
Jasmonates, Divinylethers and GLVs with
functions of GLVs. GLVs- green leaf volatiles,
PUFAs- polyunsaturated fatty acids, LOXsLipoxygenases, AOS- allene oxide synthase, DESdivinyl ether synthase, HPL- hydroperoxide lyase,
ADH- alcohol dehydrogenase.
biosynthesis, biological functions and biotechnological applications of GLVs.
Biosynthesis of GLVs
In this section, a brief description of the substrates and the
enzymes involved in the biosynthetic pathway of GLVs is
presented (Figure 1).
Phospholipases
The degradation of membrane lipids occurs under normal
conditions during physiological and developmental processes in
plants and may be initiated by biotic and abiotic stresses
(Wasternack, 2007). Previous studies have elucidated the role
of phospholipase A (PLA) enzymes in the release of free PUFAs,
which are the substrates for the oxylipin pathway. For example,
DEFECTIVE ANTHER DEHISCENCE 1 (DAD1) and DONGLE (DGL)
possess PLA1 activity and release ALA for the biosynthesis of JA
in Arabidopsis (Hyun et al., 2008; Ishiguro et al., 2001). In
addition, the Arabidopsis genome has been reported to contain
genes encoding secreted phospholipase A2 (sPLA2) and a family
of patatin-related phospholipase A (pPLA) genes (Ryu, 2004).
sPLA2 enzymes are small, calcium-dependent and strict sn2
stereo-specific proteins, but they are not related to patatin.
Patatins are potato tuber proteins that form the catalytic domain
of enzymes with acyl-hydrolysing activity in bacteria, yeast,
animals and plants. Patatin-related enzymes have been documented to participate in different cellular functions, including
lipid mobilisation during seed germination (Scherer et al., 2010).
Yang et al. (2012a) reported that pPLAs are involved in the
release of free fatty acids and monoacyl glycerol through the
hydrolysis of membrane glycerolipids (Yang et al., 2012a).
However, further studies are needed to completely understand
the mechanisms by which free PUFAs become available for the
oxylipin pathway.
Lipoxygenases
The most important enzymes of the oxylipin pathway are a family
of monomeric, nonheme iron-containing dioxygenases of
approximately 100 kDa, termed lipoxygenase enzymes (LOXs,
EC 1.13.11). The carboxy-terminal of the polypeptide chain is
comparatively larger and possesses catalytic nonheme iron, while
the amino-terminal b-barrel domain is comparatively smaller and
thought to participate in regulation of the enzyme’s activity
(Walther et al., 2011). Recently, a tyrosine residue in the aminoterminal domain was found to be strongly associated with the
carboxy-terminal subunit and is believed to play an important role
in the catalytic activity and stability of the polypeptide chain
(Shang et al., 2011). Members of this family catalyse the
formation of unsaturated fatty acid metabolites in both animals
and plants by the regio-specific and stereo-specific addition of
molecular oxygen to a (Z, Z)-1, 4-pentadiene system containing
PUFAs (Andreou and Feussner, 2009; Joo and Oh, 2012). In
plants, these fatty acid hydroperoxides further enter various
metabolic pathways to be converted into different signalling
molecules, such as GLVs and jasmonates (Farmer and Mueller,
€m and Funk,
2013; Feussner and Wasternack, 2002; Haeggstro
2011; Scala et al., 2013a; Schaller and Stintzi, 2009) (Figure 1).
Many studies have revealed that LOXs are localized in the
chloroplast in various plant species and are associated mainly with
the thylakoid membranes (Bannenberg et al., 2009; Farmaki
et al., 2007; Porta et al., 2008). With the advancement of
analytical techniques and functional genomics, researchers have
been able to identify, clone and evaluate the role of many LOX
genes from different plant species. For example, three different
types of LOXs in soya bean, six in Arabidopsis thaliana, 23 in
cucumber and 25 in apple have been studied for their role in plant
development (Bannenberg et al., 2009; Shin et al., 2008; Vogt
et al., 2013; Yang et al., 2012b). The most common substrates
for plants LOXs, which are provided by lipases through the
degradation of membrane lipids, are LA and ALA. Several studies
have shown that LOXs are quite specific towards their substrates
(Feussner and Wasternack, 2002; Liavonchanka and Feussner,
2006; Siedow, 1991).
Plant LOXs have been classified into two types: 9-LOXs are
referred to as type-1 and are localized outside the plastids;
13-LOXs are referred to as type-2 LOXs and harbour a plastidial
transit peptide. This classification is based on the regio-specific
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GLVs functions and their applications 729
oxygenation of PUFAs by LOX, which can occur at C-9 or at C-13
of the hydrocarbon backbone in the case of a C-18 fatty acid
(Schneider et al., 2007). Typically, one of the LOX isoforms is
expressed more predominantly than the others, for example the
9-LOX gene in cucumber and the 13-LOX gene in watermelon.
However, it appears that the 13-LOX pathway contributes more
strongly to the overall oxylipin pathway compared with the 9-LOX
pathway.
9-LOX (EC 1.13.11.58) are 741–886 amino acid proteins, that
share >60% amino acid sequence identity among the subclass
(Vernooy-Gerritsen et al., 1984). The existence of this enzyme has
been documented in many plant species, including Arabidopsis
thaliana (Bannenberg et al., 2009; Lang et al., 2008; Zheng and
Brash, 2010). This enzyme catalyses the oxygenation at carbon
number 9 of the hydrocarbon backbone in LA and ALA to yield
(9S, 10E, 12Z)-9-hydroperoxyoctadeca-10,12-dienoic acid (9HPOD) and (9S, 10E, 12Z, 15Z)-9-hydroperoxy-10,12,15-octadecatrienoic acid (9-HPOT), respectively (Liavonchanka and Feussner, 2006). These oxygenated intermediates are then converted
into biologically active compounds by downstream enzymes of
the oxylipin pathway (Feussner and Wasternack, 2002) (Figure 1).
The products of the 9-LOX pathway serve as key players in various
developmental processes in plants. Maize ZmLOX3, a 9-LOX,
plays an important role in the regulation of development and also
acts as a susceptibility factor (Gao et al., 2007, 2008). In the
model plant Arabidopsis thaliana, 9-LOX is involved in late root
development (Vellosillo et al., 2007). The induction of a specific
9-LOX gene has been reported to participate in potato tuber
growth, and a reduction in tuber size was observed in response to
the suppression of this gene using an antisense strategy (Kolomiets et al., 2001). Numerous previous studies have highlighted
the roles of 9-LOX products in plant defence strategies, particularly in the hypersensitive response (HR). The HR is one of the
first and most efficient resistance reactions and is characterized by
the rapid death of plant cells in the vicinity of a pathogen attack
(Cacas et al., 2005; Gobel et al., 2003; Jalloul et al., 2002;
Marmey et al., 2007; Rance et al., 1998; Rusterucci et al., 1999;
Sayegh-Alhamdia et al., 2008). In a recent study, Arabidopsis
thaliana LOX1 (9-LOX) and DOX1 (a-Dioxygenase) were shown to
possess strong antibacterial activity. Individual mutants lox1 and
dox1 and a double mutant lox1dox1 were tested to evaluate their
efficacy against Pseudomonas syringae pv. tomato (Pst) infection.
The lox1 plants exhibited an enhanced susceptibility to the
virulent strain Pst DC3000, and systemic acquired resistance (SAR)
was partially impaired in both mutants. In the lox1dox1 double
mutant plants, both the above-mentioned defects were further
enhanced. However, pretreatment of these plants with 9-LOX
and a-DOX resulted in the production of oxylipins, particularly
9-ketooctadecatrienoic acid, and protected the plant tissues
against bacterial infection (Vicente et al., 2012). The activation of
a 9-LOX gene in pepper (Capsicum annuum), designated as
CaLOX1, has been reported to positively regulate broad-spectrum
resistance and cell death in response to pathogen infection
(Hwang and Hwang, 2010). Two closely related 9-LOX paralogs
in maize, that is ZmLOX4 and ZmLOX5, respond to various
threats, such as insects, herbivory, wounding and pathogen
infection, through a unique mechanism (Park et al., 2010).
13-LOX (EC 1.13.11.12) is a subclass of the LOX family of
enzymes that contains 896 to 941 amino acids. A large variety of
plants have been reported to express 13-LOX genes, including
soya bean, cucumber, maize and Arabidopsis thaliana (Acosta
et al., 2009; Bannenberg et al., 2009; Chohany et al., 2011;
Rudolph et al., 2011). This LOX family subclass is characterized by
the oxygenation of carbon number 13 in the PUFA substrates LA
and ALA to form (9Z, 11E, 13S)-13-hydroperoxyoctadeca-9,
11-dienoic acid (13-HPOD) and (9Z, 11E, 15Z)-13-hydroperoxyoctadeca-9, 11, 15-trienoic acid (13-HPOT). The conversion of
these oxidized fatty acids to biologically active oxylipins, such as
jasmonates, GLVs and divinylethers, occurs via seven different
metabolic pathways (Andreou et al., 2009; Feussner and Wasternack, 2002; Gigot et al., 2010). These downstream products of
13-LOX metabolism serve as important components in the
regulation of gene expression for plant defence (Farmer et al.,
2003). One of the most studied and well-characterized compounds in the oxylipin pathway is the plant hormone JA, which is
formed in the leaves in response to wounding and other stimuli
(Feussner and Wasternack, 2002; Halitschke and Baldwin, 2003).
13-HPOT, which is generated by 13-LOX oxygenation of LA or
ALA, undergoes allene oxide synthase (AOS) catalysis to form
allene oxide intermediates (Tijet and Brash, 2002). Further
reactions in the JA synthesis pathway are catalysed by allene
oxide cyclase and 12-oxopendienoic acid (OPDA) reductase,
followed by 3 cycles of b-oxidation (Andreou and Feussner,
2009). Alternatively, 13-hydroperoxide lyase (13-HPL) enzymes
catalyse the conversion of 13-hydroperoxide intermediates to 6carbon aldehydes, which are believed to possess signalling
functions and play a direct role in plant defence (Bate and
Rothstein, 1998; Croft et al., 1993). Previously, 13-HPOT and 13hydroxytridecanoic acid (13-HOT) were described as antifungal
compounds and suggested for disease control in brassica plants
(Graner et al., 2003). In a recent study, 13-hydroperoxides from
papaya seedlings exhibited antifungal activity against Phytophthora palmivora by inhibiting the germination of sporangia and
the growth of mycelia (Sujatha et al., 2012). Certain LOXs can
produce both 9- and 13- hydroperoxy metabolites; for example,
LOX1, LOX2 and LOX3 in soya bean can produce 9- and 13HPODs at different pH values (Axelrod, 1981). In a recent study,
9-LOX from Nicotiana benthamiana (Nb9-LOX) was shown to
possess the specificity of both 9- and 13-LOX, with a high
predominance for the 9-LOX function. In this study, Nb9-LOX was
incubated with LA and 13-HPL from watermelon or 9/13-HPL
from melon, followed by LC–MS analysis of the products (Huang
and Schwab, 2011).
Hydroperoxide lyases
Hydroperoxide lyase (HPL) is a member of the CYP74 subfamily of
the cytochrome P450 family of enzymes. Three types of enzymes,
that is AOS, HPL and divinylether synthase (DES), are included in
the CYP74 subfamily, and the AOS and HPL genes have been
found in all sequenced plant genomes (Brash, 2009; Hughes
et al., 2009). The genes encoding HPL are found mainly in algae,
mushrooms, Penicillium and higher plants and have been
characterized and cloned in many plant species, such as cucumber, green bell pepper, tomato and alfalfa (Atwal et al., 2005;
mez et al., 2010; Wan
Noordermeer et al., 2000; Santiago-Go
et al., 2013). Most HPLs are membrane bound; HPLs in plants
such as Arabidopsis contain a chloroplast transit peptide, whereas
HPLs in other plants, such as tomato and melon, do not have a
clear transit peptide and are suggested to be microsome localized
(Bate et al., 1998; Froehlich et al., 2001; Noordermeer et al.,
2001). The structural details of plant HPLs remain poorly
understood and require further investigation. However, recent
studies have highlighted the structural aspects of HPLs in plants.
For example, the green bell pepper HPL is composed of 480
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730 Muhammad Naeem ul Hassan et al.
amino acids and has a molecular weight of approximately
55 kDa. Circular dichroism analysis demonstrated that the protein
secondary structure of dodecyl maltoside is composed of
approximately 13% a-helix, 32% b-sheet, 21% turn and 31%
mez et al.,
unordered coils (Panagakou et al., 2013; Santiago-Go
2010). Similarly, the Solanum tuberosum HPL is a protein of
approximately 54 kDa (Mu et al., 2012). The functional enzyme is
a trimer or a tetramer with an optimum pH range of 6–9.5 and an
optimum temperature of approximately 30 °C (Gigot et al.,
2010).
Depending on the specificity of the substrate, plant HPLs have
been classified into three types: 9-HPL, 13-HPL and 9/13 HPL
(Morant et al., 2003). The majority of plant HPLs are specific for
13-hydroperoxide substrates, while enzymes from a few plant
species (e.g. almond) catalyse the cleavage of 9-hydroperoxides
(Mita et al., 2005). However, the HPLs from the 9/13 HPL subclass
that can utilize both 9- and 13-hydroperoxide substrates have
recently been documented in certain plants, such as cucumber,
rice, Medicago spp. and grape (Chehab et al., 2006; De
Domenico et al., 2007; Matsui et al., 2000; Zhu et al., 2012).
HPLs catalyse the isomerisation of 9- and 13-hydroperoxides of
PUFAs, formed by the action of 9- and 13-LOXs, respectively, to
unstable hemiacetals (Grechkin et al., 2006). In the 9-HPL
pathway, these hemiacetals spontaneously decompose to yield
volatile C9 aldehydes, including cis-3-nonenal, trans-2-nonenal
and nonvolatile C9 oxoacids. In the 13-HPL pathway, fatty acid
hydroperoxide substrates undergo homolytic isomerisation
between C12 and C13 to produce unstable hemiacetals, which
spontaneously decompose to release volatile C6 aldehydes,
hexanal and (Z)-3-hexenal from LA and ALA, respectively
(Grechkin and Hamberg, 2004). Nonvolatile C12 oxoacids are
also formed in these reactions, for example 12-oxo-(Z)-9-dodecenoic acid, which is a precursor of traumatin. These aldehydes are
the parent compounds for all other C6 aldehydes, C6 alcohols
and their acetylated derivatives (D’Auria et al., 2007; Galliard
et al., 1976; Hatanaka, 1993; Shiojiri et al., 2006b). The conversion of aldehydes to alcohols is brought about by NAD-dependent
alcohol dehydrogenase (ADH) to confer higher stability (Fauconnier et al., 1999). All of these saturated and unsaturated C6/C9
aldehydes, alcohols and esters, which are synthesized in vegetative plant tissue, particularly the leaves are volatile and are
collectively referred to as GLVs. GLVs are released within seconds
in response to tissue disruption due to biotic or abiotic stresses as
a result of activation of the HPL genes (Figure 1).
Biological functions of GLVs
Different roles of GLVs in plant defence, communication and
natural aromas and flavours are presented in this section
(Table 1).
GLVs in plant defence
To maintain a healthy flora, phyto-artillery has to confront against
multiple intruders at many fronts. Oxylipin pathway is also a
component of these frontline defence mechanisms that is
activated in response to various threats, including pathogens
and herbivory (Figure 1). The phytohormone JA has been studied
extensively to determine its efficacy and mechanism in plant
defence against biotic threats. Currently, JA is considered one of
the major phytohormones involved in plant defence, together
with salicylic acid and ethylene, due to its role in inducing
resistance against necrotrophic pathogens, chewing herbivores
and certain phloem-feeding insects. Other jasmonates, including
OPDA, methyl jasmonate and L-isoleucine jasmonate, have also
gained attention in recent years for their importance in stress
signalling and SAR. As the scope of the present review is to
highlight the role of another component of the oxylipin pathway,
readers are referred to recently published review articles for a
comprehensive description of JA (De Vleesschauwer et al., 2013;
Derksen et al., 2013; Lyons et al., 2013; Wasternack and Hause,
2013; Yang et al., 2013).
The GLV/HPL pathway has recently been implicated in plant
defence and is less well understood than the JA/AOS pathway.
GLVs serve as signals of stress within a plant as well as between
neighbouring plants within a plant community. Plants emit only
trace amounts of the GLVs under normal physiological conditions;
however, under stressed conditions, these volatiles can be formed
very rapidly (Allmann and Baldwin, 2010; D’Auria et al., 2007).
Increased synthesis and emission of these compounds has been
reported under stress-related conditions such as herbivory,
pathogen attack and abiotic stimuli (Brilli et al., 2011; Fall et al.,
1999; Gomi et al., 2003; Heiden et al., 2003; Shiojiri et al.,
2006a; Turlings et al., 1995). However, numerous studies have
suggested that the two competing branches of the oxylipin
pathway crosstalk during metabolism and the stress response. In
a recent study, Christensen et al. (2013) highlighted the role of
ZmLOX10, a Zea mays LOX that provides substrates for GLV
biosynthesis, and the coordination between the GLV and JA
pathways in the defence of maize plants against insect herbivory
(Christensen et al., 2013). In addition, Liu et al. (2012) recently
reported that the AOS and HPL branches of the oxylipin pathway
crosstalk in a coordinated manner to manipulate disease resistance in rice (Liu et al., 2012). Similarly, pretreatment of
Arabidopsis plants with aldehyde GLVs, particularly (E)-2-hexenal,
enhanced the sensitivity of the plants towards methyl-jasmonate
(Hirao et al., 2012). An HPL gene (OsHPL3) in rice plants was
recently shown to modulate direct and indirect plant defences
against various biotic threats by affecting the JA and GLV levels
(Tong et al., 2012).
GLVs in plants priming and herbivore defence
Insect herbivores utilize the physical and chemical resources of the
host plants for feeding and oviposition. Generalist herbivores can
use a variety of plant species from various families for feeding
purposes, but specialist herbivores have only one or a few options
for feeding. In response to herbivory, plants produce direct
defence molecules, which act as toxins and repellents, as well as
indirect defence molecules, such as GLVs and extra-floral nectar,
which attract the natural enemies of herbivores. Interplant
communication via airborne signalling is now a well-established
phenomenon in plant science, but it remained a controversial
topic for many years. The debate over ‘talking trees’ began in the
1980s, and over the last three decades, researchers have
accumulated significant evidence to support this hypothesis. It is
now a relatively well-established theory that plants ‘eavesdrop’ on
a bouquet of volatile organic compounds (VOCs), of which GLVs
and terpenoids are the major constituents. The bouquet of
volatiles is released by plants, that is the emitters, in the plant
headspace and then into the atmosphere in response to biotic or
abiotic stresses. These volatile signals are carried by the air to
neighbouring plants, that is the receivers, which perceive the
signal and respond by activating the expression of genes related
to direct and indirect defences (Baldwin et al., 2006; Heil, 2014;
Kessler et al., 2006).
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GLVs functions and their applications 731
Table 1 Biological functions of GLVs
Biological
functions
GLVs involved/tested
Description/comments
Reference
Herbivore
(E)-2-hexenal and 3-hexen-1-ol
Volatile extracts from cucumber, cotton, tomato, tobacco, cabbage and celery were
Li et al. (2014)
defence
used to evaluate the behavioural responses of Bemisia tabaci
(E)-2-hexenal and (Z)-3-hexenyl
acetate
(Z)-3-hexenal
GLVs released in response to damage caused by herbivory were shown to attract the
Shiojiri et al. (2006b)
parasitic wasp, Cotesia glomerata, that attacks Pieris rapae larvae
The role of a rice HPL gene (OsHPL3) in resistance against white-backed
Wang et al. (2014)
planthopper is reported
GLVs blend
The involvement of rice OsHPL3 in direct and indirect defences against insect
Tong et al. (2012)
herbivores is highlighted
Nonanal
Tritrophic interactions: Colorado Potato Beetle (CPB)-infested potato plants
Gosset et al. (2009)
released GLVs, particularly nonanal, that serve as an attractants for predators
of the CPB
(Z)-3-hexenol
Activation of defence responses by GLVs against insect herbivory is reported
Engelberth et al. (2013)
in maize plants
(Z)-3-hexenol
Role by which (Z)-3-hexenol and its acetylated derivative activate defences
Farag et al. (2005)
against insect herbivory is elucidated
Hexenyl acetate
Tritrophic interactions: Indirect defence mechanisms mediated by wound-inducible
Chehab et al. (2008)
volatile signals to attract the natural enemies of plant invaders
GLVs blend
Tritrophic interactions: Tobacco plants reduced their herbivore load by releasing
Halitschke et al. (2008)
GLVs and terpenoids for attracting predatory bugs
(Z)-3-hexenol
Tritrophic interactions: (Z)-3-hexenol released from leafminer pests, Liriomyza
Wei et al. (2007)
huidobrensi-damaged plants attracted a naive parasitic wasp, Opius dissitus,
for rescue
(E)-2-hexenal
Tritrophic interactions: treatment of soya bean plants at early flowering stages
Vieira et al. (2014)
with synthetic (E)-2-hexenal attracted Trissolcus spp and other natural enemies
of stink bugs
(E)-2-hexenal, (E-2, Z-6)nonadienal and (E)-2-nonenal
Plants
(E)-2-hexenal
priming
The toxicity of GLVs was tested against three medically significant mites and
Hubert et al. (2008)
pests, and the inhibitory concentrations were optimized
Bouquet of volatiles from clipped sagebrush, including (E)-2-hexenal, successfully
Kessler et al. (2006)
primed the tobacco trypsin proteinase inhibitor response
(E)-2-hexenal
Increased sensitivity of Arabidopsis plants to MeJA was observed
Hirao et al. (2012)
Nonanal
Priming of lima bean plants through induction of LOX and PR-2 gene expression
Yi et al. (2009)
(Z)-3-hexenal, (Z)-3- hexenol
Priming of corn plants due to herbivorous insects reported
Engelberth et al. (2004)
Acetylated derivatives released by GLVs in intact maize plants induced the priming
Yan and Wang (2006)
via airborne signalling
and (Z)-3-hexenyl acetate
(Z)-3-hexenyl acetate
of neighbouring plants
GLVs blend
The intensity of GLVs and the frequency of exposure were optimized for priming
Shiojiri et al. (2012)
Arabidopsis plants
Pathogen
defence
(E)-2-hexenal and (Z)-3-hexenyl
Antifungal activity of GLVs against Botrytis cinerea identified
Shiojiri et al. (2006a)
Defence against the fungal pathogen, Aspergillus carbonarius was indicated by the
Mita et al. (2007)
acetate
C9 aldehydes
induction of 9LOX/HPL gene expression, producing C9 aldehydes in immature
almond seeds
Mixture of oxylipins
The large-scale screening of oxylipins for their antimicrobial activity against several
Prost et al. (2005)
plant pathogens was reported
(E)-2-hexenal
Fungal protein targets for C6 aldehydes were elucidated using radio-labelled
Myung et al. (2007)
aldehydes in Botrytis cinerea
C9 aldehydes
Fungicidal action against fungal pathogens, Botrytis cinerea and Fusarium oxysporum
Matsui et al. (2006)
was reported due to 9/13 HPL activity in cucumber
Constitutive and wound
induced GLVs including (Z)-
An HPL from tea, overexpressed in tomato revealed enhanced resistance against
Xin et al. (2014)
the fungal pathogen, Alternaria alternata f. sp. Lycopersici
hexenal and (Z)-3-hexen-1-ol
(E)-2-hexena1, (Z)-3-hexeno1
One of the earliest reports on the bactericidal activity of GLVs
Croft et al. (1993)
(E)-3-hexenal
Bactericidal potential of various GLVs tested against different organisms. (E)-3-hexenal
Nakamura and
was found to be the most efficient compound against many bacteria
Hatanaka (2002)
Kishimoto et al. (2008)
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
732 Muhammad Naeem ul Hassan et al.
Table 1 Continued
Biological
functions
GLVs involved/tested
Description/comments
(Z)-3-hexenal, (E)-2-hexenal,
Transgenic Arabidopsis plants with an overexpressed or suppressed HPL gene were
and n-hexanal
Reference
studied to show that C6 aldehydes have direct fungicidal activity against Botrytis
cinerea
Aroma and
flavour
C6 and C9 aldehydes
and alcohols
Changes in the contents of various GLVs were detected during the course of
Wan et al. (2013)
cucumber fruit ripening
(Z)-3-hexen-1-ol, 1-hexanol,
hexanal, (E)-2-hexenal and
Progressive replacement of the green odour with floral and sweet sensations due to
Oliveira et al. (2011)
changes in the levels of GLVs was reported during strawberry fruit ripening
hexyl acetate
Hexanal, (E)-2-hexenal,
hexanol and (Z)-3-hexenol
Hexanal and (E)-2-hexenal were found to be the major volatiles in the green
Velickovic et al. (2013)
Medlar fruit, and hexenol and (Z)-3-hexenol were the major volatiles present in
the ripe fruit
GLVs blend
Flavour- and aroma-active compounds reported in different brands of tea
Alasalvar et al. (2012)
(E)-2-Hexenal
Two strawberry cultivars were analysed to determine the major active odour
Du et al. (2011)
volatiles. (E)-2-hexenal was found to be the major volatile for ‘fresh
strawberry’ flavour
(Z)-3-hexenal and
(E)- 2-hexenal
Profiling of the aroma components in fresh cherry tomato revealed (Z)-3-hexenal
Selli et al. (2014)
and (E)-2-hexenal to be the major aroma-active compounds, with strong green
grassy and green-leafy odour, respectively
As a major component of herbivore-induced plant volatiles
(HIPVs), GLVs participate in indirect defence via tritrophic interactions and priming, a process by which HIPVs from a damaged
plant prepare neighbouring plants to defend themselves against a
future attack (Frost et al., 2008; Goellner and Conrath, 2008)
(Table 1). Herbivore dynamics may be influenced by antiherbivore
defence priming through the activation of direct and indirect
defence mechanisms via tritrophic interactions (Kaplan, 2012).
However, the amount of volatiles released from plant foliage in
response to herbivory or pathogen stresses is directly related to
the severity of the attack (Niinemets et al., 2013). In a recent
report, Shiojiri et al. (2012) optimized the concentration of GLVs
released by damaged Arabidopsis plants and the frequency of
exposure to neighbouring undamaged plants, which was required
for successful defence priming (Shiojiri et al., 2012).
Mechanical wounding of plants or attack by herbivores
activates the oxylipin pathway and initiates the synthesis of GLVs.
The emission of GLVs in response to herbivory induces indirect
defences by activating defence-related gene expression and
attracting carnivorous arthropods to locate the herbivores (Halitschke et al., 2008). The up-regulation of numerous genes
involved in direct and indirect defences has been documented in
maize plants exposed to (Z)-3-hexenol. Furthermore, it was
demonstrated that (Z)-3-hexenol is a much more powerful elicitor
of defences against insect herbivory compared with common
defence signals, such as methyl jasmonate, methyl salicylate and
ethylene (Engelberth et al., 2013).
Recent studies have elucidated the role of insect oral secretions
in promoting wound-induced responses (Erb et al., 2012; Meldau
et al., 2012). For example, herbivore-damaged lima bean plants
produced volatiles that triggered the production of extra-floral
nectar in undamaged plants. Predatory arthropods are attracted
by extra-floral nectar, which represents an induced defence
mechanism (Heil and Kost, 2006; Heil and Silva Bueno, 2007).
Resistance against bacterial blight in rice plants is induced by
white-backed planthopper (Sogatella furcifera) (Gomi et al.,
2010). Maize plants treated with three GLVs, that is, (Z)3-hexenal, (Z)-3-hexen-1-ol, and (Z)-3- hexenyl acetate, subsequently produced higher concentrations of JA than the control
plants. Furthermore, the production of HIPVs in GLV-treated
plants was enhanced in response to caterpillar regurgitant
combined with mechanical wounding (Engelberth et al., 2004).
The same GLVs were later shown to up-regulate the expression of
three genes of the octadecanoid pathway for the synthesis of JA
(Engelberth et al., 2007). Similarly, priming of HIPV emission and
up-regulation of defence gene expression was observed in
undamaged maize plants exposed to Spodoptera littoraliswounded conspecifics. Moreover, Spodoptera littoralis had lower
relative growth rates after feeding on primed maize plants, and
the bouquet of HIPVs released from these plants was more
attractive for the parasitic wasp Cotesia marginiventris (von M
erey
et al., 2013; Ton et al., 2007). (Z)-3-hexenol, a universal GLV
induced by mechanically-damaged or leafminer-damaged plants,
is suggested to be the most important general damage attractant
that helps parasitoids locate their prey or the host plant (Wei
et al., 2007). Arabidopsis plants overexpressing HPL but with
suppressed AOS (aos-OX-HPL) released higher amounts of volatile
hexenyl acetate following aphid (Myzus persicae) infestation.
Furthermore, the results of a choice assay indicated that female
Aphidius colemani, a parasitic wasp, were more attracted to GLVs
produced by these plants after mechanical damage than the
plants in which both AOS and HPL were silenced (aos-hpl) and
therefore unable to release hexenyl acetate or any other GLV
(Chehab et al., 2008). Overexpression of the bell pepper (Capsicum annuum L.) HPL gene in Arabidopsis plants renders the
plants more attractive to the parasitic wasp Cotesia glomerata
due to their enhanced production of GLVs. By contrast, the
transgenic Arabidopsis plants in which HPL was suppressed by
antisense cloning of the gene could not produce significant
amounts of GLVs and were less attractive to parasitoids, which
resulted in reduced resistance to herbivory (Shiojiri et al., 2006a).
In a recent study, the antisense expression of a rice HPL (OsHPL3)
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
GLVs functions and their applications 733
highlighted the role of one of the GLVs, that is, (Z)-3-hexenal, in
the resistance of rice plants against the white-backed planthopper (Wang et al., 2014).
GLVs in pathogen defence
Plant pathogens have been classified as either necrotrophs that
kill plant cells before feeding on the dead plant tissue or as
biotrophs that use living plant tissue for nutritional purposes
without causing any damage. To restrict the invasion and spread
of potential microbial pathogens, plants have evolved different
mechanisms as a part of their local defence and SAR strategies.
Several studies have highlighted the role of oxylipins in plant
defence against a variety of pathogens (Table 1). Prost et al.
(2005) screened numerous oxylipins for antimicrobial activity and
found that most of the oxylipins were active against eukaryotic
microbes (Prost et al., 2005). In an earlier study, two GLVs, that is
(E)-2-hexenal and (Z)-3-hexenol, exhibited bactericidal activity at
low and high concentrations, respectively (Croft et al., 1993). In
another study, the antibacterial activity of GLVs was reported
against both Gram-positive and Gram-negative bacteria (Nakamura and Hatanaka, 2002). The priming of plant resistance against
a pathogenic bacterium due to airborne plant-plant signalling was
recently reported. A natural population of lima beans (Phaseolus
lunatus) growing adjacent to conspecific neighbours that had
been chemically induced with benzothiadiazole was more resistant to infection by the bacterial pathogen Pseudomonas syringae
pv. syringae. Nonanal was identified as the major constituent in
the headspace of the plants treated with benzothiadiazole, and
the enhanced expression of genes related to PATHOGENESISRELATED PROTEIN2 (PR-2), which are likely involved in this effect,
was observed (Yi et al., 2009). Treatment with (E)-2-hexenal or
the presence of active HPL enhanced the susceptibility of
Arabidopsis plants to Pseudomonas syringae pv. tomato. This
response was mediated by ORA59, a key transcription factor in
the JA pathway (Scala et al., 2013b).
Fungicidal activity was detected in Arabidopsis thaliana plants
overexpressing the HPL gene in response to the accumulation of
higher amounts of C6 aldehydes following infection with the
plant pathogen Botrytis cinerea. However, suppression of this
gene resulted in reduced amounts of C6 aldehydes compared
with the wild type plants, and therefore less resistance to the
fungal pathogen (Kishimoto et al., 2008). In another study, the
antifungal activity of the infection site was monitored using radiolabelled C6 aldehydes that were synthesized in vitro from ALA
using LOX and HPL extracts and Botrytis cinerea. Most of the
radio-labelled C6 aldehydes were recovered from the fungal
surface proteins and mainly from the conidia rather than the
mycelia (Myung et al., 2007). Matsui et al. (2006) documented
the fungicidal activities of C6 and C9 aldehydes against two
fungal pathogens, Botrytis cinerea and Fusarium oxysporum, in
disrupted cucumber leaves (Matsui et al., 2006). A recent study
reported enhanced resistance of transgenic tomato plants with
constitutively expressed tea HPL against the necrotrophic fungus
Alternaria alternata f. sp. lycopersici (Xin et al., 2014). Certain
GLVs, such as hexanal and (E)-2-hexenal, have been implicated in
food storage due to their antimicrobial activities (Hubert et al.,
2008).
GLVs in natural aromas and flavours
Humans can sense more than 7000 volatile compounds with the
use of 347 olfactory receptors (Goff and Klee, 2006). A complex
mixture of more than 1000 volatile compounds that include
aldehydes, alcohols, esters, terpenes, and some carbonyl and
sulphur compounds impart aroma to fruits (Lara et al., 2003).
Plant volatiles serve as a source of relief and refreshment for
humans due to their aromas and odours, which is indicative of
absence of insects and harmful microorganisms (Table 1). Consumers’ choice of fruits, vegetables and processed foods depends
mainly on a blend of characteristics such as aroma, colour, odour
and flavour. Volatile compounds are synthesized in the vegetative
tissues of plants in response to biotic stresses, mainly herbivory
and pathogens (Arimura et al., 2009). The disruption of glandular
trichomes due to herbivory results in the emission of volatile
compounds at high concentrations to repel the attackers
(Schilmiller et al., 2008). These volatile compounds are important
constituents of the flavour and fresh green aroma in fruits and
vegetables and impart a characteristic odour to each plant
referred to as the ‘green note’ (Gigot et al., 2010; Hatanaka,
1993; Weichert et al., 2002).
Volatile profiling of strawberry (Arbutus unedo) fruit during
different stages of ripening showed that C6 alcohols are the
major components of the blend of volatiles, followed by
aldehydes and esters, until the final ripening stage (Oliveira et al.,
2011). The key aromatic compounds that contribute to the green,
grassy odour note of guava fruit are (Z)-3-hexenal and hexanal
(Steinhaus et al., 2009). The volatile alcohols, (Z)-2-hexenol and
(Z)-3-hexenol, and the aldehydes hexanal and (E)-2-hexenal, with
their green, grassy, sweet, fruity odour, are the major contributors of the sensory characteristics in different tea varieties
(Alasalvar et al., 2012; Borse et al., 2002; Schuh and Schieberle,
2006; Wang et al., 2011). An analysis of odourants from
strawberry indicated that ethyl hexanoate is one of the most
intense volatile esters that impart a fruity aroma (Du et al., 2011).
In a recent study, (Z)-3-hexenal and (E)-2-hexenal were identified
as the most powerful aromatic active volatiles in fresh cherry
tomato extracts (Selli et al., 2014).
Applications of GLVs in biotechnology
Natural flavour compounds share a major part of the global
market of food additives. Green note products were valued at
approximately 900 million USD in the worldwide market in 2006
and have continued to increase steadily (Xu et al., 2007).
Consumers’ demand for natural flavourants and odourants has
increased in recent years due to health and safety concerns. The
advancement of knowledge has led to new strategies for the
large-scale production of these natural food additives through
biotechnological applications. Because of the blend of inherent
green, fresh and fruity aromas, GLVs are widely applied in the
food and beverage industry (Fukushige and Hildebrand, 2005)
(Table 2).
The natural ‘fresh green’ aroma of fruits and vegetables, which
is lost during industrial processing, is reconstituted through the
application of HPL-generated volatiles (Delcarte et al., 2003).
Buchhaupt et al. (2012) described a highly efficient process for
the synthesis of green note by overexpressing soya bean LOX2
and watermelon HPL in the yeast Saccharomyces cerevisiae
(Buchhaupt et al., 2012). The production of large quantities of
hexanal, (Z)-3-hexenal and (E)-2-hexenal was achieved by designing an efficient biosynthetic strategy. A viral vector system was
used in this design to overexpress a 13-LOX gene from soya bean
(GmVLXC) and a 13-HPL gene from watermelon (ClHPL) by agroinfiltration in Nicotiana benthamiana and incubating the plant
leaf extract with LA (Huang et al., 2010). Using the same
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
734 Muhammad Naeem ul Hassan et al.
Table 2 Applications of GLVs in biotechnology
Plant/fruit (enzyme source)
Target GLVs
Process description
Reference
HPL from Amaranthus tricolor
(E)-2-hexenal
Synthesis and purification of (E)-2-hexenal, by salt-adding steam
Xiong et al. (2012)
distillation is described
HPL from sugar beet
(E)-2-hexenal
Modulated substrate addition and continuous products removal employed
Gigot et al. (2012)
for the efficient biotransformation of fatty acid hydroperoxide substrates
to GLVs
Pink guava fruit
(Z)-3-hexenal and
hexanal
13-LOX gene from Soya
bean (GmVLXC) and a 13-HPL
Hexanal, (Z)-3- hexenal
and (E)-2-hexenal
gene from watermelon
9-LOX/9-HPL, 9-LOX/tomato
Re-engineering of aroma- and odour-active compounds and omission tests
Steinhaus et al. (2009)
employed for the characterisation of guava fruit aroma
Production of large amounts of C6 aldehydes by expressing a viral vector
Huang et al. (2010)
containing soybean LOX and watermelon HPL in Nicotiana benthamiana
plants is described
C9-aldehydes
The biotransformation of LA to C9 aldehydes and trihydroxy fatty acids
peroxygenase and 9-LOX/potato
using tobacco leaf extracts is described. The tobacco plants contained
epoxide hydrolase
a recombinant viral vector with genes encoding enzymes downstream
Huang and
Schwab (2012)
of 9-LOX from different sources by agrobacterium infiltration
strategy, C9-aldehydes and trihydroxy fatty acids were produced
in large quantities by 9-LOX/9-HPL, 9-LOX/tomato peroxygenase
and 9-LOX/potato epoxide hydrolase overexpression (Huang and
Schwab, 2012). Gigot et al. (2012) devised a bioreactor for the
synthesis of original GLVs from 13-HPOT using recombinant sugar
beet HPL (BVHPL). This process was highly efficient, and
the product, that is a mixture of GLVs with (Z)-3-hexenal and
(E)-2-hexenal as the major constituents, was suggested to be of
high quality and suitable for use in foods and beverages as a
natural aroma (Gigot et al., 2012). Similarly, (E)-2-hexenal has
been synthesized from 13-HPOT and Amaranthus tricolor HPL
using a green method, followed by purification using salt-adding
steam distillation (Xiong et al., 2012).
Conclusion and future prospects
In the last few decades, numerous studies have reported on the
role of the oxylipin pathway in plant physiology and defence. As
discussed earlier in this review, a number of stresses can activate
the oxylipin pathway, resulting in the release of higher amounts
of jasmonates and GLVs, which are otherwise released in very
low concentrations (Allmann and Baldwin, 2010). The release of
higher GLV concentrations under stressed conditions led us to
conclude that gene expression for the GLV biosynthetic pathway
is induced by signals from infection or stress. However, the
nature of these signals and the mechanisms by which these stress
signals lead to the generation of the defence response remain
elusive, particularly the release of free or esterified PUFAs. New
strategies need to be devised and certain novel substrates may
need to be designed and tested to identify the ‘missing link’
between the perception of stress and the defence response in the
affected plants. The importance of GLVs in the plant response to
microbial pathogen attack has been studied since the early
1990s.
Although many studies have shown encouraging results, most
are limited to laboratory experiments that were performed using
synthetic GLVs. Further laboratory and field experiments using the
natural bouquet of these volatiles are required to comprehensively understand this process. The most interesting aspect of the
ongoing research on GLVs is their role in tri-trophic interactions
and plant-plant communication, where these compounds have
emerged as key players. Optimistically, it appears that we are
close to entering an era of understanding ‘plant psychology’,
where GLVs play a central role, similar to the nerve impulses in
the human central nervous system. Currently, most of our
knowledge on plant-insect interactions is limited to only a few
plant species, and the molecular mechanisms driving these
processes are not clear (Broekgaarden et al., 2011). However,
an extensive amount of research from different fields in the plant
and biological sciences should be integrated to understand the
language that plants use for communication within their ecosystem. Laboratory and field experiments may be designed to
evaluate and analyse these signals at the genomics, proteomics
and metabolomics levels to answer certain questions. For
example, what types of signals are involved in stress and the
associated response? What types of plants in an ecosystem
transmit signals and what types of plant receptors can receive airborne signals? How are the signals transmitted through receiver
plants, and how do they induce a pre-attack defence response?
The best solution to these questions will likely arise from a more
intensive and systematic approach that uses systems biology and
an integrative biology platform. In addition, we need a comprehensive understanding of the signalling mechanisms of these
pathways at the genetic and molecular levels. The modification of
key steps in these pathways using genetic engineering tools and
more advanced biochemical strategies, such as epigenetic alterations, could be used to firmly control the pathway switches
(Seymour et al., 2013). Enabling useful plants to produce their
own herbicides, pesticides and antimicrobials will help us eliminate the need for toxic sprays, reduce costs and protect the
environment. This strategy could be helpful for the protection of
crops and normal flora as well as the production of natural foods
with improved quality.
Acknowledgement
We would like to thank and show our appreciation to Universiti
Kebangsaan Malaysia for financing this project through
“Research University Grant (DLP-2013-008).
References
Acosta, I.F., Laparra, H., Romero, S.P., Schmelz, E., Hamberg, M., Mottinger,
J.P., Moreno, M.A. and Dellaporta, S.L. (2009) tasselseed1 is a lipoxygenase
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
GLVs functions and their applications 735
affecting jasmonic acid signaling in sex determination of maize. Science, 323,
262–265.
Alasalvar, C., Topal, B., Serpen, A., Bahar, B., Pelvan, E. and Gokmen, V. (2012)
Flavor characteristics of seven grades of black tea produced in Turkey. J.
Agric. Food Chem. 60, 6323–6332.
Allmann, S. and Baldwin, I.T. (2010) Insects betray themselves in nature to
predators by rapid isomerization of green leaf volatiles. Science, 329, 1075–
1078.
Andreou, A. and Feussner, I. (2009) Lipoxygenases – structure and reaction
mechanism. Phytochemistry, 70, 1504–1510.
Andreou, A., Brodhun, F. and Feussner, I. (2009) Biosynthesis of oxylipins in
non-mammals. Prog. Lipid Res. 48, 148–170.
Arimura, G., Matsui, K. and Takabayashi, J. (2009) Chemical and molecular
ecology of herbivore-induced plant volatiles: proximate factors and their
ultimate functions. Plant Cell Physiol. 50, 911–923.
Atwal, A.S., Bisakowski, B., Richard, S., Robert, N. and Lee, B. (2005) Cloning
and secretion of tomato hydroperoxide lyase in Pichia pastoris. Process
Biochemistry, 40(1), 95–102.
Axelrod, B. (1981) Lipoxygenase from soybeans. Methods Enzymol. 71, 441–
451.
Balbi, V. and Devoto, A. (2008) Jasmonate signalling network in Arabidopsis
thaliana: crucial regulatory nodes and new physiological scenarios. New
Phytol. 177, 301–318.
Baldwin, I.T., Halitschke, R., Paschold, A., von Dahl, C.C. and Preston, C.A.
(2006) Volatile signaling in plant-plant interactions: “talking trees” in the
Genomics Era. Science, 311, 812–815.
Bannenberg, G., Martinez, M., Hamberg, M. and Castresana, C. (2009)
Diversity of the enzymatic activity in the lipoxygenase gene family of
Arabidopsis thaliana. Lipids, 44, 85–95.
Bate, N.J. and Rothstein, S.J. (1998) C6-volatiles derived from the lipoxygenase
pathway induce a subset of defense-related genes. Plant J. 16, 561–569.
Bate, N.J., Sivasankar, S., Moxon, C., Riley, J.M., Thompson, J.E. and Rothstein,
S.J. (1998) Molecular characterization of an Arabidopsis gene encoding
hydroperoxide lyase, a cytochrome P-450 that is wound inducible. Plant
Physiol. 117, 1393–1400.
Borse, B.B., Jagan Mohan Rao, L., Nagalakshmi, S. and Krishnamurthy, N.
(2002) Fingerprint of black teas from India: identification of the regio-specific
characteristics. Food Chem. 79, 419–424.
Brash, A.R. (2009) Mechanistic aspects of CYP74 allene oxide synthases and
related cytochrome P450 enzymes. Phytochemistry, 70, 1522–1531.
Brilli, F., Ruuskanen, T.M., Schnitzhofer, R., Muller, M., Breitenlechner, M.,
Bittner, V., Wohlfahrt, G., Loreto, F. and Hansel, A. (2011) Detection of plant
volatiles after leaf wounding and darkening by proton transfer reaction
“time-of-flight” mass spectrometry (PTR-TOF). PLoS ONE, 6, e20419.
Broekgaarden, C., Snoeren, T.A., Dicke, M. and Vosman, B. (2011) Exploiting
natural variation to identify insect-resistance genes. Plant Biotechnol. J. 9,
819–825.
Buchhaupt, M., Guder, J.C., Etschmann, M.M.W. and Schrader, J. (2012)
Synthesis of green note aroma compounds by biotransformation of fatty
acids using yeast cells coexpressing lipoxygenase and hydroperoxide lyase.
Appl. Microbiol. Biotechnol. 93, 159–168.
Cacas, J.-L., Vailleau, F., Davoine, C., Ennar, N., Agnel, J.-P., Tronchet, M.,
Ponchet, M., Blein, J.-P., Roby, D., Triantaphylides, C. and Montillet, J.-L.
(2005) The combined action of 9 lipoxygenase and galactolipase is sufficient
to bring about programmed cell death during tobacco hypersensitive
response. Plant Cell Environ. 28, 1367–1378.
Chehab, E.W., Raman, G., Walley, J.W., Perea, J.V., Banu, G., Theg, S. and
Dehesh, K. (2006) Rice HYDROPEROXIDE LYASES with unique expression
patterns generate distinct aldehyde signatures in Arabidopsis. Plant Physiol.
141, 121–134.
Chehab, E.W., Kaspi, R., Savchenko, T., Rowe, H., Negre-Zakharov, F.,
Kliebenstein, D. and Dehesh, K. (2008) Distinct roles of jasmonates and
aldehydes in plant-defense responses. PLoS ONE, 3, e1904.
Chohany, L.E., Bishop, K.A., Camic, H., Sup, S.J., Findeis, P.M. and Clapp, C.H.
(2011) Cationic substrates of soybean lipoxygenase-1. Bioorg. Chem. 39, 94–
100.
Christensen, S.A., Nemchenko, A., Borrego, E., Murray, I., Sobhy, I.S., Bosak, L.,
DeBlasio, S., Erb, M., Robert, C.A. and Vaughn, K.A. (2013) The maize
lipoxygenase, ZmLOX10, mediates green leaf volatile, jasmonate and
herbivore-induced plant volatile production for defense against insect
attack. Plant J. 74, 59–73.
Croft, K., Juttner, F. and Slusarenko, A.J. (1993) Volatile products of the
lipoxygenase pathway evolved from Phaseolus vulgaris (L.) leaves
inoculated with Pseudomonas syringae pv phaseolicola. Plant Physiol.
101, 13–24.
D’Auria, J.C., Pichersky, E., Schaub, A., Hansel, A. and Gershenzon, J. (2007)
Characterization of a BAHD acyltransferase responsible for producing the
green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 49,
194–207.
De Domenico, S., Tsesmetzis, N., Di Sansebastiano, G.P., Hughes, R.K., Casey,
R. and Santino, A. (2007) Subcellular localisation of Medicago truncatula 9/
13-hydroperoxide lyase reveals a new localisation pattern and activation
mechanism for CYP74C enzymes. BMC Plant Biol. 7, 58.
De Vleesschauwer, D., Gheysen, G. and Hofte, M. (2013) Hormone defense
networking in rice: tales from a different world. Trends Plant Sci. 18, 555–
565.
Delcarte, J., Fauconnier, M., Jacques, P., Matsui, K., Thonart, P. and Marlier, M.
(2003) Optimisation of expression and immobilized metal ion affinity
chromatographic purification of recombinant (His)6-tagged cytochrome
P450 hydroperoxide lyase in Escherichia coli. J. Chromatogr. B Analyt.
Technol. Biomed. Life Sci. 786, 229–236.
Derksen, H., Rampitsch, C. and Daayf, F. (2013) Signaling cross-talk in plant
disease resistance. Plant Sci. 207, 79–87.
D’Haeze, W. and Holsters, M. (2002) Nod factor structures, responses, and
perception during initiation of nodule development. Glycobiology, 12, 79R–
105R.
Du, X., Plotto, A., Baldwin, E. and Rouseff, R. (2011) Evaluation of volatiles
from two subtropical strawberry cultivars using GC-olfactometry, GC-MS
odor activity values, and sensory analysis. J. Agric. Food Chem. 59, 12569–
12577.
Engelberth, J., Alborn, H.T., Schmelz, E.A. and Tumlinson, J.H. (2004) Airborne
signals prime plants against insect herbivore attack. Proc. Natl Acad. Sci.
U.S.A. 101, 1781–1785.
Engelberth, J., Seidl-Adams, I., Schultz, J.C. and Tumlinson, J.H. (2007) Insect
elicitors and exposure to green leafy volatiles differentially upregulate major
octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea
mays. Mol. Plant Microbe Interact. 20, 707–716.
Engelberth, J., Contreras, C.F., Dalvi, C., Li, T. and Engelberth, M. (2013) Early
transcriptome analyses of Z-3-Hexenol-treated zea mays revealed distinct
transcriptional networks and anti-herbivore defense potential of green leaf
volatiles. PLoS ONE, 8, e77465.
Erb, M., Meldau, S. and Howe, G.A. (2012) Role of phytohormones in insectspecific plant reactions. Trends Plant Sci. 17, 250–259.
Fall, R., Karl, T., Hansel, A., Jordan, A. and Lindinger, W. (1999) Volatile
organic compounds emitted after leaf wounding: on-line analysis by protontransfer-reaction mass spectrometry. J. Geophys. Res. Atmos. 104, 15963–
15974.
Farag, M.A., Fokar, M., Abd, H., Zhang, H., Allen, R.D. and Pare, P.W. (2005)
(Z)-3-Hexenol induces defense genes and downstream metabolites in maize.
Planta, 220, 900–909.
Farmaki, T., Sanmartın, M., Jimenez, P., Paneque, M., Sanz, C., Vancanneyt, G.,
n, J. and Sanchez-Serrano, J.J. (2007) Differential distribution of the
Leo
lipoxygenase pathway enzymes within potato chloroplasts. J. Exp. Bot. 58,
555–568.
Farmer, E.E. and Mueller, M.J. (2013) ROS-mediated lipid peroxidation and RESactivated signaling. Annu. Rev. Plant Biol. 64, 429–450.
Farmer, E.E., Almeras, E. and Krishnamurthy, V. (2003) Jasmonates and related
oxylipins in plant responses to pathogenesis and herbivory. Curr. Opin. Plant
Biol. 6, 372–378.
Fauconnier, M.L., Mpambara, A., Delcarte, J., Jacques, P., Thonart, P. and
Marlier, M. (1999) Conversion of green note aldehydes into alcohols by yeast
alcohol dehydrogenase. Biotechnol. Lett. 21, 629–633.
Feussner, I. and Wasternack, C. (2002) The lipoxygenase pathway. Annu. Rev.
Plant Biol. 53, 275–297.
Froehlich, J.E., Itoh, A. and Howe, G.A. (2001) Tomato allene oxide synthase
and fatty acid hydroperoxide lyase, two cytochrome P450s involved in
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
736 Muhammad Naeem ul Hassan et al.
oxylipin metabolism, are targeted to different membranes of chloroplast
envelope. Plant Physiol. 125, 306–317.
Frost, C.J., Mescher, M.C., Carlson, J.E. and De Moraes, C.M. (2008) Plant
defense priming against herbivores: getting ready for a different battle. Plant
Physiol. 146, 818–824.
Frydman, A., Weisshaus, O., Bar-Peled, M., Huhman, D.V., Sumner, L.W.,
Marin, F.R., Lewinsohn, E., Fluhr, R., Gressel, J. and Eyal, Y. (2004) Citrus fruit
bitter flavors: isolation and functional characterization of the gene
Cm1,2RhaT encoding a 1,2 rhamnosyltransferase, a key enzyme in the
biosynthesis of the bitter flavonoids of citrus. Plant J. 40, 88–100.
Fukushige, H. and Hildebrand, D.F. (2005) Watermelon (Citrullus lanatus)
hydroperoxide lyase greatly increases C6 aldehyde formation in transgenic
leaves. J. Agric. Food Chem. 53, 2046–2051.
Galliard, T., Phillips, D.R. and Reynolds, J. (1976) The formation of cis-3nonenal, trans-2-nonenal and hexanal from linoleic acid hydroperoxide
isomers by a hydroperoxide cleavage enzyme system in cucumber (Cucumis
sativus) fruits. Biochim. Biophys. Acta, 441, 181–192.
Gao, X., Shim, W.B., Gobel, C., Kunze, S., Feussner, I., Meeley, R., Balint-Kurti,
P. and Kolomiets, M. (2007) Disruption of a maize 9-lipoxygenase results in
increased resistance to fungal pathogens and reduced levels of
contamination with mycotoxin fumonisin. Mol. Plant Microbe Interact. 20,
922–933.
Gao, X., Starr, J., Gobel, C., Engelberth, J., Feussner, I., Tumlinson, J. and
Kolomiets, M. (2008) Maize 9-lipoxygenase ZmLOX3 controls development,
root-specific expression of defense genes, and resistance to root-knot
nematodes. Mol. Plant Microbe Interact. 21, 98–109.
Gershenzon, J. (2007) Plant volatiles carry both public and private messages.
Proc. Natl Acad. Sci. U.S.A. 104, 5257–5258.
Gigot, C., Ongena, M., Fauconnier, M.-L., Wathelet, J.-P., Du Jardin, P. and
Thonart, P. (2010) The lipoxygenase metabolic pathway in plants: potential
for industrial production of natural green leaf volatiles. Biotechnol. Agron.
Soc. Environ. 14, 451–460.
Gigot, C., Ongena, M., Fauconnier, M.-L., Muhovski, Y., Wathelet, J.-P., du
Jardin, P. and Thonart, P. (2012) Optimization and scaling up of a
biotechnological synthesis of natural green leaf volatiles using Beta vulgaris
hydroperoxide lyase. Process Biochem. 47, 2547–2551.
Gobel, C., Feussner, I. and Rosahl, S. (2003) Lipid peroxidation during the
hypersensitive response in potato in the absence of 9-lipoxygenases. J. Biol.
Chem. 278, 52834–52840.
Goellner, K. and Conrath, U. (2008) Priming: it’s all the world to induced
disease resistance. Eur. J. Plant Pathol. 121, 233–242.
Goff, S.A. and Klee, H.J. (2006) Plant volatile compounds: sensory cues for
health and nutritional value? Science, 311, 815–819.
Gomi, K., Yamasaki, Y., Yamamoto, H. and Akimitsu, K. (2003)
Characterization of a hydroperoxide lyase gene and effect of C6-volatiles
on expression of genes of the oxylipin metabolism in Citrus. J. Plant Physiol.
160, 1219–1231.
Gomi, K., Satoh, M., Ozawa, R., Shinonaga, Y., Sanada, S., Sasaki, K.,
Matsumura, M., Ohashi, Y., Kanno, H., Akimitsu, K. and Takabayashi, J.
(2010) Role of hydroperoxide lyase in white-backed planthopper (Sogatella
furcifera Horvath)-induced resistance to bacterial blight in rice, Oryza sativa L.
Plant J. 61, 46–57.
€bel, C., Francis, F., Haubruge, E., Wathelet, J.-P., Du
Gosset, V., Harmel, N., Go
Jardin, P., Feussner, I. and Fauconnier, M.-L. (2009) Attacks by a piercingsucking insect (Myzus persicae Sultzer) or a chewing insect (Leptinotarsa
decemlineata Say) on potato plants (Solanum tuberosum L.) induce
differential changes in volatile compound release and oxylipin synthesis. J.
Exp. Bot. 60(4), 1231–40, erp015.
Graner, G., Hamberg, M. and Meijer, J. (2003) Screening of oxylipins for control
of oilseed rape (Brassica napus) fungal pathogens. Phytochemistry, 63, 89–
95.
Grechkin, A.N. and Hamberg, M. (2004) The “heterolytic hydroperoxide lyase”
is an isomerase producing a short-lived fatty acid hemiacetal. Biochim.
Biophys. Acta, 1636, 47–58.
Grechkin, A.N., Bruhlmann, F., Mukhtarova, L.S., Gogolev, Y.V. and Hamberg,
M. (2006) Hydroperoxide lyases (CYP74C and CYP74B) catalyze the
homolytic isomerization of fatty acid hydroperoxides into hemiacetals.
Biochim. Biophys. Acta, 1761, 1419–1428.
€m, J.Z. and Funk, C.D. (2011) Lipoxygenase and leukotriene
Haeggstro
pathways: biochemistry, biology, and roles in disease. Chem. Rev. 111,
5866–5898.
Halitschke, R. and Baldwin, I.T. (2003) Antisense LOX expression increases
herbivore performance by decreasing defense responses and inhibiting
growth-related transcriptional reorganization in Nicotiana attenuata. Plant J.
36, 794–807.
Halitschke, R., Stenberg, J.A., Kessler, D., Kessler, A. and Baldwin, I.T. (2008)
Shared signals –‘alarm calls’ from plants increase apparency to herbivores and
their enemies in nature. Ecol. Lett. 11, 24–34.
Hatanaka, A. (1993) The biogeneration of green odour by green leaves.
Phytochemistry, 34, 1201–1218.
Heiden, A.C., Kobel, K., Langebartels, C., Schuh-Thomas, G. and Wildt, J.
(2003) Emissions of oxygenated volatile organic compounds from plants part
I: emissions from lipoxygenase activity. J. Atmos. Chem. 45, 143–172.
Heil, M. (2014) Herbivore-induced plant volatiles: targets, perception and
unanswered questions. New Phytol. 204, 297–306.
Heil, M. and Kost, C. (2006) Priming of indirect defences. Ecol. Lett. 9, 813–817.
Heil, M. and Silva Bueno, J.C. (2007) Within-plant signaling by volatiles leads to
induction and priming of an indirect plant defense in nature. Proc. Natl Acad.
Sci. U.S.A. 104, 5467–5472.
€nsche, H., Fang, J., Baldwin, I.T.
Heinrich, M., Hettenhausen, C., Lange, T., Wu
and Wu, J. (2013) High levels of jasmonic acid antagonize the biosynthesis of
gibberellins and inhibit the growth of Nicotiana attenuata stems. Plant J. 73,
591–606.
Hirao, T., Okazawa, A., Harada, K., Kobayashi, A., Muranaka, T. and Hirata, K.
(2012) Green leaf volatiles enhance methyl jasmonate response in
Arabidopsis. J. Biosci. Bioeng. 114, 540–545.
Huang, F.C. and Schwab, W. (2011) Cloning and characterization of a 9lipoxygenase gene induced by pathogen attack from Nicotiana benthamiana
for biotechnological application. BMC Biotechnol. 11, 30.
Huang, F.C. and Schwab, W. (2012) Overexpression of hydroperoxide lyase,
peroxygenase and epoxide hydrolase in tobacco for the biotechnological
production of flavours and polymer precursors. Plant Biotechnol. J. 10, 1099–
1109.
Huang, F.C., Studart-Witkowski, C. and Schwab, W. (2010) Overexpression of
hydroperoxide lyase gene in Nicotiana benthamiana using a viral vector
system. Plant Biotechnol. J. 8, 783–795.
Hubert, J., Munzbergova, Z., Nesvorna, M., Poltronieri, P. and Santino, A.
(2008) Acaricidal effects of natural six-carbon and nine-carbon aldehydes on
stored-product mites. Exp. Appl. Acarol. 44, 315–321.
Hughes, R.K., De Domenico, S. and Santino, A. (2009) Plant cytochrome CYP74
family: biochemical features, endocellular localisation, activation mechanism
in plant defence and improvements for industrial applications.
ChemBioChem, 10, 1122–1133.
Hwang, I.S. and Hwang, B.K. (2010) The pepper 9-lipoxygenase gene CaLOX1
functions in defense and cell death responses to microbial pathogens. Plant
Physiol. 152, 948–967.
Hyun, Y., Choi, S., Hwang, H.-J., Yu, J., Nam, S.-J., Ko, J., Park, J.-Y., Seo, Y.S.,
Kim, E.Y., Ryu, S.B., Kim, W.T., Lee, Y.-H., Kang, H. and Lee, I. (2008)
Cooperation and functional diversification of two closely related galactolipase
genes for jasmonate biosynthesis. Dev. Cell, 14, 183–192.
Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I. and Okada, K. (2001) The
DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase
A1 catalyzing the initial step of jasmonic acid biosynthesis, which
synchronizes pollen maturation, anther dehiscence, and flower opening in
Arabidopsis. Plant Cell, 13, 2191–2209.
Jalloul, A., Montillet, J.L., Assigbetse, K., Agnel, J.P., Delannoy, E.,
Triantaphylides, C., Daniel, J.F., Marmey, P., Geiger, J.P. and Nicole, M.
(2002) Lipid peroxidation in cotton: Xanthomonas interactions and the role of
lipoxygenases during the hypersensitive reaction. Plant J. 32, 1–12.
Joo, Y.-C. and Oh, D.-K. (2012) Lipoxygenases: potential starting biocatalysts
for the synthesis of signaling compounds. Biotechnol. Adv. 30, 1524–1532.
Kaplan, I. (2012) Attracting carnivorous arthropods with plant volatiles: the
future of biocontrol or playing with fire? Biol. Control, 60, 77–89.
Kessler, A., Halitschke, R. and Baldwin, I.T. (2004) Silencing the jasmonate
cascade: induced plant defenses and insect populations. Science, 305, 665–
668.
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
GLVs functions and their applications 737
Kessler, A., Halitschke, R., Diezel, C. and Baldwin, I.T. (2006) Priming of plant
defense responses in nature by airborne signaling between Artemisia
tridentata and Nicotiana attenuata. Oecologia, 148, 280–292.
Kishimoto, K., Matsui, K., Ozawa, R. and Takabayashi, J. (2008) Direct
fungicidal activities of C6-aldehydes are important constituents for defense
responses in Arabidopsis against Botrytis cinerea. Phytochemistry, 69, 2127–
2132.
Kolomiets, M.V., Hannapel, D.J., Chen, H., Tymeson, M. and Gladon, R.J.
(2001) Lipoxygenase is involved in the control of potato tuber development.
Plant Cell, 13, 613–626.
Lang, I., Gobel, C., Porzel, A., Heilmann, I. and Feussner, I. (2008) A
lipoxygenase with linoleate diol synthase activity from Nostoc sp. PCC
7120. Biochem. J. 410, 347–357.
Lange, B.M. and Ahkami, A. (2013) Metabolic engineering of plant
monoterpenes, sesquiterpenes and diterpenes–current status and future
opportunities. Plant Biotechnol. J. 11, 169–196.
, R.M., Fuentes, T., Sayez, G., Graell, J. and Lo
pez, M.L. (2003)
Lara, I., Miro
Biosynthesis of volatile aroma compounds in pear fruit stored under longterm controlled-atmosphere conditions. Postharvest Biol. Technol. 29, 29–39.
Li, Y., Zhong, S., Qin, Y., Zhang, S., Gao, Z., Dang, Z. and Pan, W. (2014)
Identification of plant chemicals attracting and repelling whiteflies.
Arthropod Plant Interact. 8, 183–190.
Liavonchanka, A. and Feussner, I. (2006) Lipoxygenases: occurrence, functions
and catalysis. J. Plant Physiol. 163, 348–357.
Liechti, R. and Farmer, E.E. (2003) The Jasmonate Biochemical Pathway.
Liechti, R. and Farmer, E.E. (2006) Jasmonate Biochemical Pathway.
Liechti, R., Gfeller, A. and Farmer, E.E. (2006) Jasmonate Signaling Pathway.
Liu, X., Li, F., Tang, J., Wang, W., Zhang, F., Wang, G., Chu, J., Yan, C.,
Wang, T., Chu, C. and Li, C. (2012) Activation of the jasmonic acid
pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk
between the HPL and AOS branches of the oxylipin pathway in rice. PLoS
ONE, 7, e50089.
Lyons, R., Manners, J.M. and Kazan, K. (2013) Jasmonate biosynthesis and
signaling in monocots: a comparative overview. Plant Cell Rep. 32, 815–827.
Marmey, P., Jalloul, A., Alhamdia, M., Assigbetse, K., Cacas, J.L., Voloudakis,
A.E., Champion, A., Clerivet, A., Montillet, J.L. and Nicole, M. (2007) The 9lipoxygenase GhLOX1 gene is associated with the hypersensitive reaction of
cotton Gossypium hirsutum to Xanthomonas campestris pv malvacearum.
Plant Physiol. Biochem. 45, 596–606.
Matsui, K. (2006) Green leaf volatiles: hydroperoxide lyase pathway of oxylipin
metabolism. Curr. Opin. Plant Biol. 9, 274–280.
Matsui, K., Ujita, C., Fujimoto, S., Wilkinson, J., Hiatt, B., Knauf, V., Kajiwara, T.
and Feussner, I. (2000) Fatty acid 9- and 13-hydroperoxide lyases from
cucumber. FEBS Lett. 481, 183–188.
Matsui, K., Minami, A., Hornung, E., Shibata, H., Kishimoto, K., Ahnert, V.,
Kindl, H., Kajiwara, T. and Feussner, I. (2006) Biosynthesis of fatty acid
derived aldehydes is induced upon mechanical wounding and its products
show fungicidal activities in cucumber. Phytochemistry, 67, 649–657.
Meldau, S., Erb, M. and Baldwin, I.T. (2012) Defence on demand: mechanisms
behind optimal defence patterns. Ann. Bot. 110, 1503–1514.
von M
erey, G.E., Veyrat, N., D’Alessandro, M. and Turlings, T.C. (2013)
Herbivore-induced maize leaf volatiles affect attraction and feeding behavior
of Spodoptera littoralis caterpillars. Front. Plant Sci. 4:209. doi: 10.3389/
fpls.2013.00209.
Mita, G., Quarta, A., Fasano, P., De Paolis, A., Di Sansebastiano, G.P., Perrotta,
C., Iannacone, R., Belfield, E., Hughes, R., Tsesmetzis, N., Casey, R. and
Santino, A. (2005) Molecular cloning and characterization of an almond 9hydroperoxide lyase, a new CYP74 targeted to lipid bodies. J. Exp. Bot. 56,
2321–2333.
Mita, G., Fasano, P., De Domenico, S., Perrone, G., Epifani, F., Iannacone, R.,
Casey, R. and Santino, A. (2007) 9-Lipoxygenase metabolism is involved in
the almond/Aspergillus carbonarius interaction. J. Exp. Bot. 58, 1803–1811.
Morant, M., Bak, S., Moller, B.L. and Werck-Reichhart, D. (2003) Plant
cytochromes P450: tools for pharmacology, plant protection and
phytoremediation. Curr. Opin. Biotechnol. 14, 151–162.
Mu, W., Xue, Q., Jiang, B. and Hua, Y. (2012) Molecular cloning, expression,
and enzymatic characterization of Solanum tuberosum hydroperoxide lyase.
Eur. Food Res. Technol. 234, 723–731.
Myung, K., Hamilton-Kemp, T.R. and Archbold, D.D. (2007) Interaction with
and effects on the profile of proteins of Botrytis cinerea by C6 aldehydes. J.
Agric. Food Chem. 55, 2182–2188.
Nakamura, S. and Hatanaka, A. (2002) Green-leaf-derived C6-aroma
compounds with potent antibacterial action that act on both Gramnegative and Gram-positive bacteria. J. Agric. Food Chem. 50, 7639–7644.
€ K€annaste, A. and Copolovici, L. (2013) Quantitative patterns
Niinemets, U.,
between plant volatile emissions induced by biotic stresses and the degree of
damage. Front. Plant Sci. 4:262. doi: 10.3389/fpls.2013.00262.
Noordermeer, M.A., Van Dijken, A.J., Smeekens, S.C., Veldink, G.A. and
Vliegenthart, J.F. (2000) Characterization of three cloned and expressed 13hydroperoxide lyase isoenzymes from alfalfa with unusual N-terminal
sequences and different enzyme kinetics. Eur J Biochem. 267(9), 2473–82.
Noordermeer, M.A., Veldink, G.A. and Vliegenthart, J.F. (2001) Fatty acid
hydroperoxide lyase: a plant cytochrome p450 enzyme involved in wound
healing and pest resistance. ChemBioChem, 2, 494–504.
Oliveira, I., Guedes de Pinho, P., Malheiro, R., Baptista, P. and Pereira, J.A.
(2011) Volatile profile of Arbutus unedo L. fruits through ripening stage. Food
Chem. 128, 667–673.
Panagakou, I., Touloupakis, E. and Ghanotakis, D.F. (2013) Structural
characterization of hydroperoxide lyase in dodecyl maltoside by using
circular dichroism. Protein J. 32, 1–6.
Park, Y.S., Kunze, S., Ni, X., Feussner, I. and Kolomiets, M.V. (2010)
Comparative molecular and biochemical characterization of segmentally
duplicated 9-lipoxygenase genes ZmLOX4 and ZmLOX5 of maize. Planta,
231, 1425–1437.
Porta, H., Figueroa-Balderas, R. and Rocha-Sosa, M. (2008) Wounding and
pathogen infection induce a chloroplast-targeted lipoxygenase in the
common bean (Phaseolus vulgaris L.). Planta, 227, 363–373.
Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M.J., Kift, N., Carbonne,
F., Griffiths, G., Esquerre-Tugaye, M.-T. and Rosahl, S. (2005) Evaluation of
the antimicrobial activities of plant oxylipins supports their involvement in
defense against pathogens. Plant Physiol. 139, 1902–1913.
Rance, I., Fournier, J. and Esquerre-Tugaye, M.T. (1998) The incompatible
interaction between Phytophthora parasitica var. nicotianae race 0 and
tobacco is suppressed in transgenic plants expressing antisense lipoxygenase
sequences. Proc. Natl Acad. Sci. U.S.A. 95, 6554–6559.
Rudolph, M., Schlereth, A., Korner, M., Feussner, K., Berndt, E., Melzer, M.,
Hornung, E. and Feussner, I. (2011) The lipoxygenase-dependent oxygenation
of lipid body membranes is promoted by a patatin-type phospholipase in
cucumber cotyledons. J. Exp. Bot. 62, 749–760.
Rusterucci, C., Montillet, J.L., Agnel, J.P., Battesti, C., Alonso, B., Knoll, A.,
Bessoule, J.J., Etienne, P., Suty, L., Blein, J.P. and Triantaphylides, C. (1999)
Involvement of lipoxygenase-dependent production of fatty acid
hydroperoxides in the development of the hypersensitive cell death induced
by cryptogein on tobacco leaves. J. Biol. Chem. 274, 36446–36455.
Ryu, S.B. (2004) Phospholipid-derived signaling mediated by phospholipase A in
plants. Trends Plant Sci. 9, 229–235.
mez, M.P., Kermasha, S., Nicaud, J.-M., Belin, J.-M. and Husson, F.
Santiago-Go
(2010) Predicted secondary structure of hydroperoxide lyase from green bell
pepper cloned in the yeast Yarrowia lipolytica. J. Mol. Catal. B Enzym. 65, 63–
67.
Sayegh-Alhamdia, M., Marmey, P., Jalloul, A., Champion, A., Petitot, A.S.,
Clerivet, A. and Nicole, M. (2008) Association of lipoxygenase response with
resistance of various cotton genotypes to the bacterial blight disease. J.
Phytopathol. 156, 542–549.
Scala, A., Allmann, S., Mirabella, R., Haring, M. and Schuurink, R. (2013a)
Green leaf volatiles: a plant’s multifunctional weapon against herbivores and
pathogens. Int. J. Mol. Sci. 14, 17781–17811.
Scala, A., Mirabella, R., Mugo, C., Matsui, K., Haring, M.A. and Schuurink, R.C.
(2013b) E-2-hexenal promotes susceptibility to Pseudomonas syringae by
activating jasmonic acid pathways in Arabidopsis. Front. Plant Sci. 4:74. doi:
10.3389/fpls.2013.00074.
Schaller, A. and Stintzi, A. (2009) Enzymes in jasmonate biosynthesis –
structure, function, regulation. Phytochemistry, 70, 1532–1538.
Scherer, G.F.E., Ryu, S.B., Wang, X., Matos, A.R. and Heitz, T. (2010) Patatinrelated phospholipase A: nomenclature, subfamilies and functions in plants.
Trends Plant Sci. 15, 693–700.
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
738 Muhammad Naeem ul Hassan et al.
Schilmiller, A.L., Last, R.L. and Pichersky, E. (2008) Harnessing plant trichome
biochemistry for the production of useful compounds. Plant J. 54, 702–711.
Schneider, C., Pratt, D.A., Porter, N.A. and Brash, A.R. (2007) Control of
oxygenation in lipoxygenase and cyclooxygenase catalysis. Chem. Biol. 14,
473–488.
Schuh, C. and Schieberle, P. (2006) Characterization of the key aroma
compounds in the beverage prepared from Darjeeling black tea: quantitative
differences between tea leaves and infusion. J. Agric. Food Chem. 54, 916–
924.
Selli, S., Kelebek, H., Ayseli, M.T. and Tokbas, H. (2014) Characterization of the
most aroma-active compounds in cherry tomato by application of the aroma
extract dilution analysis. Food Chem. 165, 540–546.
Seymour, G.B., Chapman, N.H., Chew, B.L. and Rose, J.K. (2013) Regulation of
ripening and opportunities for control in tomato and other fruits. Plant
Biotechnol. J. 11, 269–278.
Shang, W., Ivanov, I., Svergun, D.I., Borbulevych, O.Y., Aleem, A.M., Stehling,
€hn, H. and Skrzypczak-Jankun, E. (2011) Probing
S., Jankun, J., Ku
dimerization and structural flexibility of mammalian lipoxygenases by smallangle X-ray scattering. J. Mol. Biol. 409, 654–668.
Shin, J.H., Van, K., Kim, D.H., Kim, K.D., Jang, Y.E., Choi, B.-S., Kim, M.Y. and
Lee, S.-H. (2008) The lipoxygenase gene family: a genomic fossil of shared
polyploidy between Glycine max and Medicago truncatula. BMC Plant Biol. 8,
133.
Shiojiri, K., Kishimoto, K., Ozawa, R., Kugimiya, S., Urashimo, S., Arimura, G.,
Horiuchi, J., Nishioka, T., Matsui, K. and Takabayashi, J. (2006a) Changing
green leaf volatile biosynthesis in plants: an approach for improving plant
resistance against both herbivores and pathogens. Proc. Natl Acad. Sci.
U.S.A. 103, 16672–16676.
Shiojiri, K., Ozawa, R., Matsui, K., Kishimoto, K., Kugimiya, S. and Takabayashi,
J. (2006b) Role of the lipoxygenase/lyase pathway of host-food plants in the
host searching behavior of two parasitoid species, Cotesia glomerata and
Cotesia plutellae. J. Chem. Ecol. 32, 969–979.
Shiojiri, K., Ozawa, R., Matsui, K., Sabelis, M.W. and Takabayashi, J. (2012)
Intermittent exposure to traces of green leaf volatiles triggers a plant
response. Sci. Rep. 2:378. doi: 10.1038/srep00378.
Siedow, J.N. (1991) Plant lipoxygenase: structure and function. Annu. Rev. Plant
Physiol. Plant Mol. Biol. 42, 145–188.
Steinhaus, M., Sinuco, D., Polster, J., Osorio, C. and Schieberle, P. (2009)
Characterization of the key aroma compounds in pink guava (Psidium
guajava L.) by means of aroma re-engineering experiments and omission
tests. J. Agric. Food Chem. 57, 2882–2888.
Sujatha, B., Devi, P. and Maheswari, U. (2012) Antifungal potential of papaya
lipoxygenase metabolites against Phytophthora palmivora. J. Pure Appl.
Microbiol. 6, 433–438.
Tijet, N. and Brash, A.R. (2002) Allene oxide synthases and allene oxides.
Prostaglandins Other Lipid Mediat. 68–69, 423–431.
Ton, J., D’Alessandro, M., Jourdie, V., Jakab, G., Karlen, D., Held, M., MauchMani, B. and Turlings, T.C. (2007) Priming by airborne signals boosts direct
and indirect resistance in maize. Plant J. 49, 16–26.
Tong, X., Qi, J., Zhu, X., Mao, B., Zeng, L., Wang, B., Li, Q., Zhou, G., Xu, X. and
Lou, Y. (2012) The rice hydroperoxide lyase OsHPL3 functions in defense
responses by modulating the oxylipin pathway. Plant J. 71, 763–775.
Turlings, T.C., Loughrin, J.H., McCall, P.J., Rose, U.S., Lewis, W.J. and
Tumlinson, J.H. (1995) How caterpillar-damaged plants protect themselves
by attracting parasitic wasps. Proc. Natl Acad. Sci. U.S.A. 92, 4169–4174.
D., Nikicevic, N.J., Zivkovic,
Velickovic, M.M., Radivojevic, D.D., Oparnica, C.
M.B., Dordevi
c, N.O., Vajs, V.E. and Tesevic, V.V. (2013) Volatile compounds
in Medlar fruit (Mespilus germanica L.) at two ripening stages. Hemijska
industrija, 67, 437–441.
Vellosillo, T., Martinez, M., Lopez, M.A., Vicente, J., Cascon, T., Dolan, L.,
Hamberg, M. and Castresana, C. (2007) Oxylipins produced by the 9lipoxygenase pathway in Arabidopsis regulate lateral root development and
defense responses through a specific signaling cascade. Plant Cell, 19, 831–
846.
Verdonk, J.C., Ric de Vos, C.H., Verhoeven, H.A., Haring, M.A., van Tunen, A.J.
and Schuurink, R.C. (2003) Regulation of floral scent production in petunia
revealed by targeted metabolomics. Phytochemistry, 62, 997–1008.
Vernooy-Gerritsen, M., Leunissen, J.L.M., Veldink, G.A. and Vliegenthart, J.F.G.
(1984) Intracellular localization of lipoxygenases-1 and -2 in germinating
soybean seeds by indirect labeling with protein A-colloidal gold complexes.
Plant Physiol. 76, 1070–1078.
Vicente, J., Cascon, T., Vicedo, B., Garcia-Agustin, P., Hamberg, M. and
Castresana, C. (2012) Role of 9-lipoxygenase and alpha-dioxygenase oxylipin
pathways as modulators of local and systemic defense. Mol. Plant, 5, 914–
928.
Vieira, C.R., Blassioli-Moraes, M.C., Borges, M., Pires, C.S.S., Sujii, E.R. and
Laumann, R.A. (2014) Field evaluation of (E)-2-hexenal efficacy for behavioral
manipulation of egg parasitoids in soybean. Biocontrol, 59, 525–537.
Vogt, J., Schiller, D., Ulrich, D., Schwab, W. and Dunemann, F. (2013)
Identification of lipoxygenase (LOX) genes putatively involved in fruit flavour
formation in apple (Malus 9 domestica). Tree Genet. Genomes, 9, 1493–
1511.
€hn, H. (2011) The
Walther, M., Hofheinz, K., Vogel, R., Roffeis, J. and Ku
N-terminal b-barrel domain of mammalian lipoxygenases including
mouse 5-lipoxygenase is not essential for catalytic activity and membrane
binding but exhibits regulatory functions. Arch. Biochem. Biophys. 516,
1–9.
Wan, X.H., Chen, S.X., Wang, C.Y., Zhang, R.R., Cheng, S.Q., Meng, H.W. and
Shen, X.Q. (2013) Isolation, expression, and characterization of a
hydroperoxide lyase gene from cucumber. Int. J. Mol. Sci. 14, 22082–22101.
Wang, K., Liu, F., Liu, Z., Huang, J., Xu, Z., Li, Y., Chen, J., Gong, Y. and Yang,
X. (2011) Comparison of catechins and volatile compounds among
different types of tea using high performance liquid chromatograph and
gas chromatograph mass spectrometer. Int. J. Food Sci. Technol. 46, 1406–
1412.
Wang, B., Zhou, G., Xin, Z., Ji, R. and Lou, Y. (2014) (Z)-3-hexenal, one of the
green leaf volatiles, increases susceptibility of rice to the white-backed
planthopper Sogatella furcifera. Plant Mol. Biol. Rep. doi: 10.1007/s11105014-0756-7.
Wasternack, C. (2007) Jasmonates: an update on biosynthesis, signal
transduction and action in plant stress response, growth and development.
Ann. Bot. 100, 681–697.
Wasternack, C. and Hause, B. (2013) Jasmonates: biosynthesis, perception,
signal transduction and action in plant stress response, growth and
development. An update to the 2007 review in Annals of Botany. Ann.
Bot. 111, 1021–1058.
Wei, J., Wang, L., Zhu, J., Zhang, S., Nandi, O.I. and Kang, L. (2007) Plants
attract parasitic wasps to defend themselves against insect pests by releasing
hexenol. PLoS ONE, 2, e852.
Weichert, H., Kolbe, A., Kraus, A., Wasternack, C. and Feussner, I. (2002)
Metabolic profiling of oxylipins in germinating cucumber seedlings–
lipoxygenase-dependent degradation of triacylglycerols and biosynthesis of
volatile aldehydes. Planta, 215, 612–619.
Xin, Z., Zhang, L., Zhang, Z., Chen, Z. and Sun, X. (2014) A tea hydroperoxide
lyase gene, CsiHPL1, regulates tomato defense response against Prodenia
litura (Fabricius) and Alternaria alternata f. sp. Lycopersici by modulating
green leaf volatiles (GLVs) release and jasmonic acid (JA) gene expression.
Plant Mol. Biol. Rep. 32, 62–69.
Xiong, J., Kong, X., Zhang, C., Chen, Y. and Hua, Y. (2012) Production of (2E)hexenal by a hydroperoxide lyase from Amaranthus tricolor and salt-adding
steam distillation for the separation. Eur. Food Res. Technol. 235, 783–792.
Xu, P., Hua, D. and Ma, C. (2007) Microbial transformation of
propenylbenzenes for natural flavour production. Trends Biotechnol. 25,
571–576.
Yan, Z.-G. and Wang, C.-Z. (2006) Wound-induced green leaf volatiles cause
the release of acetylated derivatives and a terpenoid in maize.
Phytochemistry, 67, 34–42.
Yang, W.-Y., Zheng, Y., Bahn, S.C., Pan, X.-Q., Li, M.-Y., Vu, H.S., Roth, M.R.,
Scheu, B., Welti, R., Hong, Y.-Y. and Wang, X.-M. (2012a) The patatincontaining phospholipase A pPLAIIa modulates oxylipin formation and water
loss in Arabidopsis thaliana. Mol. Plant, 5(2), 452–60 doi: 10.1093/mp/
ssr118.
Yang, X.-Y., Jiang, W.-J. and Yu, H.-J. (2012b) The expression profiling of the
lipoxygenase (LOX) family genes during fruit development, abiotic stress and
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739
GLVs functions and their applications 739
hormonal treatments in cucumber (Cucumis sativus L.). Int. J. Mol. Sci. 13,
2481–2500.
Yang, D.L., Yang, Y. and He, Z. (2013) Roles of plant hormones and their
interplay in rice immunity. Mol. Plant, 6, 675–685.
Yi, H.S., Heil, M., Adame-Alvarez, R.M., Ballhorn, D.J. and Ryu, C.M. (2009)
Airborne induction and priming of plant defenses against a bacterial
pathogen. Plant Physiol. 151, 2152–2161.
Zheng, Y. and Brash, A.R. (2010) On the role of molecular oxygen in
lipoxygenase activation: comparison and contrast of epidermal lipoxygenase3 with soybean lipoxygenase-1. J. Biol. Chem. 285, 39876–39887.
Zhu, B.Q., Xu, X.Q., Wu, Y.W., Duan, C.Q. and Pan, Q.H. (2012) Isolation and
characterization of two hydroperoxide lyase genes from grape berries: HPL
isogenes in Vitis vinifera grapes. Mol. Biol. Rep. 39, 7443–7455.
ª 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd, Plant Biotechnology Journal, 13, 727–739